Associations Between Pressure Pain Threshold in the Neck and Postural Control in Patients with Dizziness Or Neck Pain

Knapstad et al. BMC Musculoskeletal Disorders (2019) 20:528 https://doi.org/10.1186/s12891-019-2922-4

RESEARCH ARTICLE Open Access Associations between pressure pain threshold in the neck and postural control in patients with dizziness or neck pain – a cross-sectional study Mari K. Knapstad1,2* , Frederik K. Goplen1,2, Tove Ask3, Jan S. Skouen4,5 and Stein Helge G. Nordahl1,2

Abstract Background: It is theorized that neck pain may cause reduced postural control due to the known physiological connection between the receptors in the cervical spine and the vestibular system. The purpose of this study was to examine whether the pressure pain threshold in the neck is associated with postural sway in patients with dizziness or neck pain. Methods: Consecutive patients with dizziness (n = 243) and neck pain (n = 129) were recruited from an otorhinolaryngological department and an outpatient spine clinic, respectively. All subjects underwent static posturography. Pressure pain thresholds were measured at four standardized points in the neck, and generalized pain was assessed using the American College of Rheumatology tender points. The relationship between postural sway and pressure pain threshold was analyzed by linear regression, and the covariates included age, sex, and generalized pain. Results: In the dizzy group, there was a small, inverse relationship between pressure pain thresholds and sway area with eyes closed, after adjusting for age, sex, and generalized pain (bare platform; lower neck, p = 0.002, R2 = 0.068; upper neck, p = 0.038, R2 = 0.047; foam rubber mat; lower neck, p = 0.014, R2 = 0.085). The same inverse relationship was found between pressure pain thresholds in the neck and the Romberg ratio on a bare platform after adjusting for age, sex and generalized pain (upper neck, p = 0.15, R2 = 0.053; lower neck, p =0.002,R2 = 0.069). Neither of these relationships were present in the neck pain group. Conclusion: Our findings indicate that the pressure pain threshold in the neck is associated with postural sway in patients suffering from dizziness after adjusting for age, sex, and generalized pain, but only with closed eyes. The association was small and should be interpreted with caution. Trial registration: Trial registration: Clinicaltrial.gov NCT03531619. Retrospectively registered 22 May 2018. Keywords: Posturography, Neck pain, Dizziness

* Correspondence: [email protected] 1Norwegian National Advisory Unit on Vestibular Disorders, Department of Otorhinolaryngology & Head and Neck Surgery, Haukeland University Hospital, Jonas Lies vei 65, 5021 Bergen, Norway 2Department of Clinical Medicine, University of Bergen, Bergen, Norway Full list of author information is available at the end of the article

© The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Knapstad et al. BMC Musculoskeletal Disorders (2019) 20:528 Page 2 of 9

Background dizzy patients as many patients with dizziness suffer Postural control is a complex system [1] and to maintain from neck pain [19, 20]. Exploring this relationship in control, the body requires input from the vestibular, both patients with dizziness and patients with neck pain visual, and somatosensory systems. As part of the may provide information on how the degree of neck somatosensory system, the proprioceptive system in the pain influences postural control in two patient groups cervical spine is vital for fine tuning orientation and known to have altered balance. balance [2]. This proprioceptive system consists of the Self-reported pain intensity has been the most common deep cervical muscles, particularly the segmental mus- approach to pain measurement. While self-reported pain cles of the upper spine – with an abundance of muscle is indeed important, it is mediated by biopsychosocial spindles – in addition to mechanoreceptors from joints aspects [21] that can make it difficult to interpret. The and tendons. This system is important for both the pressure pain threshold (PPT) is a tool of both self-report stability and the mobility of the different regions in the but additionally a more objective technique [22]thatis neck. The cervical receptors provide afferent information used to quantify mechanical pain sensitivity [23, 24]. It is to the central nervous system on the orientation of the defined as the minimal amount of pressure that first head with respect to the rest of the body via modulation becomes on of pain [25]. of vestibular and visual afferent information [3]. Integra- The main aim of this study is to examine whether tion of symmetrical afferent input from the cervical, there is an association between PPT and postural sway vestibular, and visual systems in the vestibular nuclei in patients with dizziness and in patients with neck pain. complex is vital for normal head perception and postural As patients with pain syndromes, such as Fibromyalgia, control, and for providing responses resulting in precise have been shown to have reduced balance [26, 27] and motor commands to the eyes and body [3, 4]. Thus, it is patients rarely have isolated neck pain as it is usually a theorized that an asymmetry or disturbance of inputs part of a wider pain pattern [28], we wanted to adjust from cervical receptors might lead to a feeling of for generalized pain. Finally, we wanted to examine the imbalance or dizziness [3, 4]. The mechanism by which upper and lower regions of the cervical spine separately reduced cervical proprioception might lead to sensory due to their differences in mechanical properties and disturbances and reduced postural control is still uncer- distribution of mechanoreceptors. tain and disputed, even though the confluence of vestibular and cervical afferents in the brain is well Methods known [5]. It has, however, been proposed that pain, Design and setting either as a primary or secondary event, may lead to We conducted a prospective cross-sectional study of con- altered sensitivity of the muscle spindles and mechano- secutive outpatients examined at two clinical centers at a receptors due to ischemic or inflammatory events [6]. university hospital in Norway. The first center was an ear- Further, pain may cause maladaptive strategies and nose-throat (ENT) clinic that receives referrals from change the neck muscle coordination and reduce the general practitioners and specialists, both nationally and specificity of neck muscle activation, for instance, locally, concerning dizziness of suspected vestibular origin. through reduced activation of the deep segmental mus- The second center was an outpatient spine clinic that cles and increased activation of the superficial muscles admits patients from primary care physicians concerning [7]. Pain may also alter the cortical representation and long-lasting musculoskeletal pain either causing or threat- modulation of the cervical afferent input [8]. The rela- ening to cause work disability. tionship between altered neck proprioception and pain has been found in healthy subjects receiving injections Participants to induce neck pain [9], and animal studies have shown During a one-year period (2017–2018), we included con- that local injections, nerve blockades, and dissection of secutive patients examined in both clinics. The recruit- neck muscle in the upper cervical region, lead to de- ment is illustrated in Fig. 1. Patients with dizziness as creased balance, coordination, ataxia, and even nystag- their primary complaint (n = 243) were recruited from mus [10–12]. Lastly, both patients with chronic neck the ENT clinic. The ENT clinic also receives tertiary re- pain and whiplash-related disorders have been found to ferrals nationally and is a quaternary referral center for have reduced postural control [13], and the same has vestibular schwannomas and for divers suffering from been found in patients with dizziness of suspected cer- vestibular problems. As we wanted the study population vical origin [14–18]. The relationship has previously to be representative of secondary referrals, persons hav- been mostly studied in patients with neck pain; however, ing the latter conditions were not invited to participate it is not established whether the degree of neck pain is (based on medical records) and only locally referred pa- associated with the degree of postural control. It is also tients from western Norway were included. They were not known if neck pain influences postural control in diagnosed by an otorhinolaryngologist, and the examination Knapstad et al. 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Fig. 1 Recruitment process included pure-tone audiometry, dynamic posturography, neck) and bilaterally at the anterior aspects of the inter- videonystagmography with measurements of ocular smooth transverse space at C5–C7 (lower neck). The algometer pursuit, saccades and bithermal caloric tests, a standard has been shown to be a reliable tool on these sites in dizzy ENT examination including otomicroscopy, examination of patients with intraclass correlation values of 0.82–0.90 on cranial nerves and cerebellar function as well as clinical intrarater reliability and 0.85–0.91 on test–retest reliabil- tests of postural sway, gait, and nystagmus. In addition, hos- ity. The minimal detectable change showed values from pitalized patients with acute vertigo were also excluded. 44.5 kPa – 86.1 kPa on intrarater reliability and 77.7 kPa – Patients with long-lasting (> 3 months) neck pain (n = 88.2 kPa on test–retest reliability [30]. Prior to the study, 129) as their primary complaint were recruited from the the examiners practiced applying pressure at a rate of ap- outpatient spine clinic where they were examined by a proximately 50 kPa/s. The digital force gage maintained multidisciplinary team and diagnosed by a physician. In its peak value, and the examiner was blinded to the display both groups, the participants had to be between 18 and while applying pressure. The patient was told to immedi- 67 years old. Exclusion criteria included language bar- ately state when the pressure sensation changed into a riers associated with filling in patient questionnaires and pain sensation, at which time the pressure was stopped neurological or orthopedic disorders known to interfere and the score was noted. A lower score indicated a greater with postural control (these were excluded prior to degree of pain sensitivity. Three measurements were re- invitation to participate based on medical records). The corded at each site, starting on the left at the suboccipital project was approved by the Regional Committee for site and ending on the right on the intertransverse space Health and Medical Research Ethics of South-Eastern at C5–C6. As the last two measurements have been found Norway (REK 2017/783). The participants signed a to have the highest reliability [30], we used the mean of written consent prior to testing. those measures for further analysis.

Pressure pain threshold Generalized pain Neck PPT were used to quantify the mechanical pain Pressure testing at the 18 ACR tender points was used to sensitivity of the cervical region using a pressure alg- measure the level of generalized pain. The test assesses nine ometer. This threshold has previously been found to defined points on each side of the body as illustrated in predict shoulder/neck pain [29] and to correlate with Wolfe et al. (1990) [31]. The tester gradually administered other measures of neck pain [30]. The PPT was mea- increasing pressure to each point, stopping at approxi- sured in all subjects in the prone position by trained mately 4 kg pressure. The patient was told to say “yes” if physiotherapists. A Wagner FDX-25 digital force gage they experienced pain or “no” if they experienced only dis- (Wagner Instruments, Greenwich, CT) with a linear re- comfort at each point after pressure was applied. The num- sponse of 0–1300 kilopascals (kPa) and a 1 cm2 round beroftenderpoints(0–18) was used in further analysis. rubber tip was used to apply pressure to the upper four standardized and defined American College of Rheuma- Postural control tology (ACR) tender points [31]: bilaterally suboccipital Postural control was evaluated by static posturography and 2 cm lateral to the spinous process of the axis (upper using a commercially available force platform (Synapsys, Knapstad et al. BMC Musculoskeletal Disorders (2019) 20:528 Page 4 of 9

Marseille, France). The center of pressure under the feet of predictors; thus, resulting in a sample size of at least was sampled at a rate of 100 Hz. The evaluated param- 105 patients for each regression analysis. Sway area and eter was the sway area in mm2 described by the center Romberg ratio were positively skewed and were logarith- of pressure during each test lasting 2 × 20 s. The patients mically transformed prior to regression analysis. PPT in were instructed to stand quietly on the force platform the upper and lower neck was highly correlated and thus with their arms hanging freely along their body and their assessed in separate analyses to avoid multicollinearity. To feet aligned with markings corresponding to their foot facilitate interpretation of the coefficients, they were back size. To evaluate the different contributions of proprio- transformed after analysis. Statistical analysis was per- ceptive and visual inputs, the patients were tested under formed using Stata® version 15 (StataCorp, Texas, USA). four different conditions: eyes open or eyes closed while standing on the bare platform and eyes open or closed while standing on a foam rubber mat placed on top of Results the platform. Additionally, as an indicator of the pro- This study included 243 patients from the ENT clinic prioceptive contribution to postural stability the Rom- with dizziness and 129 patients from the spine clinic berg ratio [32] was calculated as the sway area with eyes with neck pain. Due to technical issues, three patients closed divided by the sway area with eyes open with and from the ENT clinic and four patients from the spine without the foam rubber on the platform. A higher ratio, clinic had to be excluded because of missing posturogra- and thus greater difference between eyes closed and eyes phy data. In addition, five patients from the ENT clinic open, indicates greater proprioceptive deficit as they rely were excluded due to neurological or orthopedic disor- more on vision to maintain postural control. ders that were not uncovered prior to participation in the study. Diagnoses of the different populations are Procedure sequence shown in Additional file 1: Table S1. In the neck pain A study nurse at each clinic recruited the patients the same group, only 17% (21 patients) reported a neck injury as day as their appointment at their respective clinic. Four ex- the trigger for their neck pain. Descriptive statistics are perienced physiotherapists conducted subsequent testing given in Table 1. on the day of their appointment. To ensure consistent PPT was not significantly associated with postural examination techniques, the examiners had two practice sway with eyes open with or without the foam mat in sessions before the study and one more after 5 months. Be- any of the groups. After adjusting for age, sex, and gen- fore testing, the participants filled in medical chart data eralized pain, there was an inverse relationship between such as age, sex, and symptom characteristics. The examin- PPT and sway area in both the eyes closed conditions ation was carried out in the following sequence: PPT, ACR (with and without foam) in the lower neck in the dizzi- tender points, and posturography. At the ENT clinic, the ness group. An increase of 10 kPa was associated with a patients were examined before or after their physician ap- 3.1% reduction of sway in the eyes closed condition pointment, and at the outpatient spine clinic the patients (95% confidence interval [CI], − 5.0 to − 1.1%, p = 0.002) were tested as a part of the physiotherapy examination and and a 1.8% reduction of sway in the eyes closed on foam after they were examined by a physician. condition (95% confidence interval [CI], − 3.3 to − 0.4%, p = 0.014). In the upper neck, there was an inverse rela- Statistical analysis tionship between PPT and sway area in the third model, Linear regression was used to estimate the relationship when standing with eyes closed on bare platform and an between postural sway (sway area and Romberg ratio) increase of 10 kPa was associated with a 1.6% reduction and PPT after adjusting for age, sex, and generalized of sway in the eyes closed condition (95% confidence pain (number of ACR tender points). Sway area was interval [CI], − 3.1 to − 0.1%, p = 0.038). In the patients used as the dependent variable and PPT as the predictor with neck pain, PPT was not associated with postural variable. Three regression models were generated, in- sway in any of the models (Table 2). cluding the unadjusted model (Model 1), the age and Regression analysis adjusted for age, sex, and general- sex-adjusted model (Model 2), and the age, sex, and gen- ized pain found an inverse relationship between PPT eralized pain-adjusted model (Model 3). The alpha level and Romberg ratio in both the upper and lower neck on was set to 0.05. Descriptive statistics included means the bare platform in the dizziness group. A 10 kPa in- and standard deviations for normally distributed data or crease in PPT in the upper neck was associated with a median and interquartile range for skewed data. Cat- 1.1% decrease in Romberg ratio (95% confidence interval egorical data were presented as percentages. The sample [CI], − 2.0 to − 0.2%, p = 0.015) and a 1.8% decrease in size was estimated based on recommendations by Green PPT in the lower neck (95% confidence interval [CI], − [33], which state that for a power of 0.8 the minimum 3.0 to − 0.7%, p = 0.002). On foam rubber, the PPT was sample size should be 104 + m where m is the number only associated with the Romberg ratio in the age and Knapstad et al. BMC Musculoskeletal Disorders (2019) 20:528 Page 5 of 9

Table 1 Descriptive data on postural control, neck PPT, and generalized pain Variable Dizziness group (n = 235) Neck pain group (n = 125) Age 45.7 ± 12 41 ± 11 Sex (female) (%) 73.5% 79.2% Duration dizziness, monthsa 12 (6–38) Duration neck pain, monthsa 14 (5–89) Concurrent complaints (%) 53% 45% Posturographya, sway area, mm2 -Eyes open; bare platform 226 (148–419) 144 (93–212) -Eyes closed; bare platform 403 (243–904) 213 (124–328) -Eyes open; foam mat 544 (346–887) 277 (194–368) -Eyes closed; foam mat 1662 (1019–2956) 639 (432–1028) Romberg ratioa,c -Bare platform 1.85 (1.13–2.74) 1.49 (1.07–1.98) -Foam mat 3.12 (2.19–4.39) 2.26 (1.71–3.14) PPT, kPab -Upper neck 216.7 ± 112.8 219.3 ± 115.8 -Lower neck 184.0 ± 86.4 192.8 ± 96.6 Generalized pain (ACR count) 9.2 ± 5.9 7.7 ± 4.9 aReported as median and interquartile range, bReported as mean and standard deviation, cRomberg ratio = sway area with eyes closed divided by sway area with eyes open. PPT Pressure pain threshold, ACR American College of Rheumatology tender points, n sample size. Concurrent complaints presence of both dizziness and neck pain the last 14 days sex-adjusted model. No relationship was found in the psychosocial factors [35]. PPT cannot directly measure neck pain group in either of the conditions (Table 3). altered proprioception of the neck, but the theory is that pain in the neck region influences the afferent input, Discussion and previous studies have supported this [8, 36]. This study found an inverse relationship between PPT in An association between postural sway and PPT was the neck, postural sway, and Romberg ratio. The effect found in patients examined for dizziness at the ENT clinic. of PPT on sway was small and the association was only This is an interesting finding. Postural control relies on present in the eyes closed conditions and only in several sensory systems, and a deficit in one of these may patients examined at the ENT clinic for dizziness. The be compensated for by the others. In the ENT clinic, ap- inverse relationship indicated that a higher PPT (lower proximately 50% were diagnosed with a vestibular prob- pain sensitivity) was associated with better performance lem. A possible explanation for our findings in this group (lower sway area and lower Romberg ratio) on the plat- may be that there was a synergistic interaction between form, and thus, a lower PPT (higher pain sensitivity) was neck pathology and vestibular deficit. Neck pain alone associated with worse performance (higher sway area may not be sufficient to cause an association between and higher Romberg ratio). The associations tended to neck pain and postural imbalance. However, 45% in the remain significant after adjustment for age, sex, and neck pain group reported dizziness. It may be speculated generalized pain. that dizziness in most of these patients was non- Previous studies have demonstrated impairments of vestibular, possibly related to their neck pain. postural control in patients with assumed cervicogenic After adjusting for age, sex, and generalized pain, the dizziness [14–18] and in neck pain patients [13]. How- association with PPT in the neck was only present with ever, these studies did not analyse the quantitative rela- eyes closed, i.e. when the patients were deprived of vis- tionship between the degree of neck pain and postural ual feedback. In the eyes closed condition, the central control, nor did they adjust for generalized pain. Ruhe nervous system has to rely on accurate vestibular and et al. (2013) found a linear relationship between the nu- somatosensory feedback, including important informa- meric pain rating scale and postural sway in patients tion about head-on-body position from proprioceptive with non-specific neck pain [34]. However, in theory, afferents in the neck [37]. This is corroborated by the PPT might be a more objective surrogate measure of association between PPT and Romberg ratio. The pain than a subjective rating because subjective mea- Romberg ratio is considered to be an indication of visual sures may be more influenced by both physiological and dependency due to proprioceptive deficit [32], and we Knapstad et al. BMC Musculoskeletal Disorders (2019) 20:528 Page 6 of 9

Table 2 Linear regression analysis between the logarithm of sway area and neck PPT in persons with dizziness (n = 234) and in persons with neck pain (n = 125) PPT Upper Neck PPT Lower Neck Groups B(CI) p R2 B (CI) p R2 Eyes open Model 1: Unadjusted Neck Pain −.0001 (−.0013 to .0010) .815 .0004 −.0003 (−.0018 to .0011) .637 .0020 Dizziness −.0002 (−.0013 to .0007) .569 .0014 −.0007 (−.0021 to .0005) .258 .0055 Model 2: Adjusted for age and Neck Pain −.0005 (−.0018 to .0008) .5436 .0468 −.0007 (−.0023 to .0008) .363 .0485 Dizziness −.0007 (−.0018to .0003) .181 .0318 −.0014 (−.0028 to <−.0001) .047 .0409 Model 3: Adjusted for age, sex, and GP Neck Pain −.0003 (−.0017 to .0010) .625 .0495 −.0005 (−.0022 to .0012) .548 .0504 Dizziness −.0004(−.0016 to .0007) .432 .0357 −.0011(−.0027 to .0093) .124 .0431 Eyes open on foam Model 1: Unadjusted Neck Pain <.0001(−.0009 to .0009) .977 <.0001 <−.0001 (−.0012 to .0011) .930 .0001 Dizziness −.0002 (−.0013 to .0007) .555 .0015 −.0001 (−.0013 to .0009) .769 .0004 Model 2: Adjusted for age and sex Neck Pain −.0001 (−.0012 to .0009) .780 .0492 −.0002 (−.0014 to .0011) .799 .0491 Dizziness −.0006 (−.0016 to .0004) .263 .0295 −.0012 (−.0026 to .0001) .086 .0367 Model 3: Adjusted for age, sex, and GP Neck Pain .0001 (−.0010 to .0012) .838 .0602 .0002 (−.0011 to .0016) .764 .0606 Dizziness −.0003 (−.0015 to .0009) .626 .0345 −.0009 (−.0024 to .0006) .234 .0394 Eyes closed Model 1: Unadjusted Neck Pain −.0003 (−.0017 to .0009) .592 .0023 −.0004 (−.0021 to .0011) .601 .0022 Dizziness −.0015 (−.0027 to −.0002) .020 .0230 −.0026 (−.0042 to −.0009) .002 .0408 Model 2: Adjusted for age and sex Neck Pain −.0005 (−.0019 to .0009) .471 .0786 −.0004 (−.0021 to .0012) .613 .0766 Dizziness −.0018 (−.0032 to −.0004) .010 .0460 −.0031 (−.0049 to −.0013) .001 .0682 Model 3: Adjusted for age, sex, and GP Neck Pain −.0004 (−.0019 to .0011) .592 .0794 −.0002 (−.0021 to .0016) .781 .0778 Dizziness −.0016 (−.0031 to <−.0001) .038 .0468 −.0031 (−.0050 to −.0011) .002 .0681 Eyes closed on foam Model 1: Unadjusted Neck Pain −.0001 (−.0012 to .0010) .837 .0003 −.0002 (−.0015 to .0012) .792 .0006 Dizziness −.0008 (−.0017 to .0002) .131 .0098 −.0014 (−.0027 to −.0002) .028 .0206 Model 2: Adjusted for age and sex Neck Pain −.0008 (−.0019 to .0004) .190 .1254 −.0008 (−.0022 to .0006) .243 .1228 Dizziness −.0011 (−.0022 to −.0002) .024 .0659 −.0021 (−.0034 to −.0008) .002 .0837 Model 3: Adjusted for age, sex, and GP Neck Pain −.0003 (−.0015 to .0009) .638 .1517 −.0003 (−.0017 to .0014) .841 .1504 Dizziness −.0009 (−.0020 to .0003) .134 .0700 −.0018 (−.0033 to −.0004) .014 .0852 PPT Pressure pain threshold, R2 explained R-squared, pp-value, CI confidence interval, B regression coefficient, n sample size, GP generalized pain (number of ACR tender points) Figures in bold indicate significant p-value Knapstad et al. BMC Musculoskeletal Disorders (2019) 20:528 Page 7 of 9

Table 3 Linear regression analysis between the logarithm of the Romberg ratio and neck PPT in persons with dizziness (n = 234) and in patients with neck pain (n = 125) PPT Upper Neck PPT Lower Neck Groups B (CI) p R2 B (CI) p R2 Romberg ratio Model 1: Unadjusted Neck Pain −.0002 (−.0011 to .0007) .620 .0020 <−.0001 (−.0011 to .0009) .881 .0002 Dizziness −.0012 (−.0019 to −.0004) .002 .0413 −.0018 (−.0029 to −.0009) <.001 .0571 Model 2: Adjusted for age and sex Neck Pain <−.0001 (−.0009 to .0009) .989 .0423 .0002 (−.0009 to .0014) .625 .0442 Dizziness −.0010 (−.0018 to −.0002) .011 .0519 −.0017 (−.0028 to −.0006) .002 .0667 Model 3: adjusted for age, sex, and GP Neck Pain <−.0001 (−.0011 to .0009) .894 .0430 .0002 (−.0009 to .0014) .625 .0442 Dizziness −.0011 (−.0020 to −.0002) .015 .0533 −.0018 (−.0030 to −.0007) .002 .0687 Romberg ratio on foam Model 1: Unadjusted Neck Pain −.0001 (−.0009 to .0007) .749 .0008 −.0001 (−.0012 to .0008) .795 .0006 Dizziness −.0005(−.0011 to .0002) .143 .0092 −.0007 (−.0015 to .0009) .082 .0130 Model 2: Adjusted for age and sex Neck Pain −.0006 (−.0015 to .0002) .154 .0746 −.0006 (−.0016to .0004) .207 .0712 Dizziness −.0005 (−.0012 to <.0001) .082 .0212 −.0009 (−.0017 to <−.0001) .039 .0264 Model 3: Adjusted for age, sex, and GP Neck Pain −.0004 (−.0013 to .0005) .383 .0845 −.0003 (−.0014 to .0008) .530 .0817 Dizziness −.0005 (−.0013 to .0002) .120 .0206 −.0009 (−.0018 to <.0001) .057 .0258 PPT Pressure pain threshold, R2 explained R-squared, p p-value, CI confidence interval, B regression coefficient, n sample size, GP generalized pain (number of ACR tender points) Figures in bold indicate significant p-value found that a reduction in the Romberg ratio (less sway choose not to rely on proprioceptive information from difference between eyes closed and eyes open) was asso- the neck as well as from the feet. The finding of a rela- ciated with an increase in PPT in both the upper and tionship between sway area and PPT in this condition, lower neck. Seemingly, patients with a higher PPT had a might indicate that neck proprioception still contrib- smaller ratio between the eyes closed and eyes open con- utes to postural stability when standing on foam rub- ditions. A possible interpretation of our findings is that a ber. However, it is important to emphasize that PPT lower PPT in the neck is associated with less reliable had a small explanatory power for both sway area and cervical proprioceptive information and thus higher vis- Romberg ratio, thus interpretation must be done with ual dependency, therefore causing increased sway in the caution. The coefficients of the association were small eyes closed condition compared to the eyes open condi- with small changes in percentage of sway. Previous tion. Other sensory deficits could affect the ratio such as studies examining PPT in the neck area found a min- degree of vestibular dysfunction. However, such mea- imal detectable change ranging from 69 to 113 kPa [30, sures do not seem to associate well with postural control 40]. Larger differences in PPT would cause a larger [38]. PPT was not associated with postural sway in the percentage of sway. In addition, it is mostly assumed eyes open conditions either with or without the foam that dizziness with a suspected cervical origin rarely mat; however, standing steadiness with eyes open is involves true vertigo and is often characterized with quite robust in patients with vestibular disorders and in more vaguely described dizziness, such as a feeling of those with proprioceptive disorders [39]. Posturography unsteadiness, disequilibrium, or light-headedness [4, with eyes closed when standing on foam rubber is con- 41]. In light of this, it is interesting to speculate sidered mostly to rely on vestibular function because vi- whether the association found in this study, however sion is eliminated and proprioceptive feedback from the small, might influence a patient’ssymptomsandafeel- feet is unreliable [39]. In this condition, the brain might ing of unsteadiness. Knapstad et al. BMC Musculoskeletal Disorders (2019) 20:528 Page 8 of 9

The relationship between sway area and PPT was most dizziness and neck pain, i.e. the patients were not se- consistent in the lower neck. This was somewhat contra- lected due to any a priori assumption of a causal link dictory to the fact that the mechanoreceptors are more between their neck symptoms and dizziness. concentrated in the upper region of the cervical spine [3]. The PPT was lower in the lower neck region in both Conclusion the dizziness group and neck pain group compared to This study found an inverse relationship between PPT the upper region. One explanation might be that the and postural sway. The association was present with eyes upper region is the most mobile part of the vertebral closed in patients suffering from dizziness after adjust- column, lack of motor control due to pain might cause ment for age, sex, and generalized pain (ACR tender the lower region of the cervical spine to compensate, points). In addition, the Romberg ratio was associated and thus increase stiffness or pain sensitivity in the with PPT. However, altered postural control has a myr- lower cervical spine. Additionally, it is important to note iad of possible causes and the effect of PPT on sway was that the PPT was measured at standardized sites, and small and needs to be corroborated in future studies. therefore perhaps not at the sites that patients perceived to be most painful. Supplementary information This study has several limitations. First, the coeffi- Supplementary information accompanies this paper at https://doi.org/10. cients of the association were small with small changes 1186/s12891-019-2922-4. in percentage of sway. In addition, the small explana- 2 Additional file 1: Table S1. Frequency of diagnosis of 231 patients tory power (R ) shows that the PPT has small effects referred to the ENT clinic and the 125 patients referred to the outpatient on sway. Although a small significant association was spine clinic. found, there is no consensus on normative values for the sway area; thus, making an interpretation of the Abbreviations importance of the percentage change difficult. How- ACR: American College of Rheumatology; COP: center of pressure; PPT: pressure pain threshold ever, the aim of this paper was merely to determine whether an association exists between PPT and sway Acknowledgments area. The relationship between neck pain and reduced The authors wish to thank the study nurses and physiotherapists at both clinics for contributing in the recruitment and assessment of participants in postural control is founded on basic research and ex- this study. perimental evidence showing that the activity of primary vestibular neurons is modulated by proprio- Authors’ contributions ceptive afferents in the neck [9–12, 42]makingita MK conducted the statistical analysis, analyzed the results, and drafted the first version of the manuscript. MK, FG, TA, JS, and SN critically interpreted plausible explanation for our findings. The populations the data and edited the manuscript. All authors read and approved the final in this study were heterogeneous as we examined the version of the manuscript. associations in symptom complexes and not specific Funding diagnoses. Persons with traumatic neck pain were un- The University of Bergen are funding the open access article processing derrepresented in the neck pain group. Even though charges of this paper. The funding sources did not influence study design, reduced postural control has been linked to neck pain collection, analysis and interpretation of data, writing, or the decision to submit the manuscript for publication. of non-traumatic origin, it might be more common in patients with traumatic origin of neck pain [13]. Pa- Availability of data and materials tients referred to the clinics with vestibular schwanno- The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request. mas, diving related inner ear trauma, severe neurologic or orthopedic injuries or referred from other parts of Ethics approval and consent to participate the country were excluded based on the medical refer- The Regional Committee for Health and Medical Research Ethics Norway approved the study (REK 2017/783). The participants signed a written ral prior to their visit. However, we did not register consent prior to testing. Study participation was voluntary with the option to how many patients were excluded prior to their visit withdraw/drop-out at any time. based on referral information. Still, if any patient reported any severe neurological or orthopedic injury Consent for publication Not applicable. after inclusion, they were registered and excluded. Finally, to examine the same association in a control Competing interests group would have enhanced this study. A strength of The authors declare that they have no competing interests. thestudywasthelargesamplesizeandthecorrection Author details for generalized pain, emphasizing the cervical contri- 1Norwegian National Advisory Unit on Vestibular Disorders, Department of bution to postural control. Moreover, the measure- Otorhinolaryngology & Head and Neck Surgery, Haukeland University Hospital, Jonas Lies vei 65, 5021 Bergen, Norway. 2Department of Clinical ments of PPT and postural sway were objective and Medicine, University of Bergen, Bergen, Norway. 3Department of Physical were performed on two unselected patient groups with Therapy, Haukeland University Hospital, Bergen, Norway. 4Department of Knapstad et al. BMC Musculoskeletal Disorders (2019) 20:528 Page 9 of 9

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